The membrane fusion step of vaccinia virus entry is cooperatively mediated by multiple viral proteins and host cell components

PLoS Pathogens

Volumn 7, Issue 12, 2011, Pages

  Laliberte, Jason P ^a   Weisberg, Andrea S ^a   Moss, Bernard ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CHOLESTEROL; CORE PROTEIN; FIREFLY LUCIFERASE; FLUORESCENT DYE; GUANOSINE TRIPHOSPHATASE; MONOCLONAL ANTIBODY; VIRUS PROTEIN; MEMBRANE PROTEIN;

ACIDIFICATION; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOSOME; HOST CELL; HUMAN; HUMAN CELL; MEMBRANE FUSION; NONHUMAN; VACCINIA VIRUS; VIRION; VIRUS ENTRY; VIRUS ENVELOPE; ANIMAL; CELL LINE; ENDOCYTOSIS; GENETICS; METABOLISM; PATHOGENICITY; PH; PHYSIOLOGY; VIROLOGY;

POXVIRIDAE; VACCINIA VIRUS;

ANIMALS; CELL LINE; CELL MEMBRANE; ENDOCYTOSIS; HUMANS; HYDROGEN-ION CONCENTRATION; MEMBRANE FUSION; MEMBRANE PROTEINS; VACCINIA VIRUS; VIRAL PROTEINS; VIRION; VIRUS INTERNALIZATION;

EID: 84855274274     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002446     Document Type: Article

References (80)

1. Chernomordik LV, Kozlov MM, (2005) Membrane hemifusion: crossing a chasm in two leaps. Cell 123: 375-382.
2. White JM, Delos SE, Brecher M, Schornberg K, (2008) Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit Rev Biochem Mol Biol 43: 189-219.
3. Heldwein EE, Krummenacher C, (2008) Entry of herpesviruses into mammalian cells. Cell Mol Life Sci 65: 1653-1668.
4. Armstrong JA, Metz DH, Young MR, (1973) The mode of entry of vaccinia virus into L cells. J Gen Virol 21: 533-537.
5. Carter GC, Law M, Hollinshead M, Smith GL, (2005) Entry of the vaccinia virus intracellular mature virion and its interactions with glycosaminoglycans. J Gen Virol 86: 1279-1290.
6. Townsley AC, Weisberg AS, Wagenaar TR, Moss B, (2006) Vaccinia virus entry into cells via a low pH-dependent-endosomal pathway. J Virol 80: 8899-8908.
7. Bengali Z, Townsley AC, Moss B, (2009) Vaccinia virus strain differences in cell attachment and entry. Virology 389: 132-140.
8. Whitbeck JC, Foo C-H, Ponce de Leon M, Eisenberg RJ, Cohen GH, (2009) Vaccinia virus exhibits cell-type-dependent entry characteristics. Virology 385: 383-391.
9. Bengali Z, Satheshkumar PS, Yang Z, Weisberg AS, Paran N, et al. (2011) Drosophila S2 cells are non-permissive for vaccinia virus DNA replication following entry via low pH-dependent endocytosis and early transcription. PLoS One 6: e17248.
10. Moss B, (2006) Poxvirus entry and membrane fusion. Virology 344: 48-54.
11. Mercer J, Helenius A, (2008) Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320: 531-535.
12. Mercer J, Knebel S, Schmidt FI, Crouse J, Burkard C, et al. (2010) Vaccinia virus strains use distinct forms of macropinocytosis for host-cell entry. Proc Natl Acad Sci USA 107: 9346-9351.
13. Moser TS, Jones RG, Thompson CB, Coyne CB, Cherry S, (2010) A kinome RNAi screen identified AMPK as promoting poxvirus entry through the control of actin dynamics. PLoS Pathog 6: e1000954.
14. Sandgren KJ, Wilkinson J, Miranda-Saksena M, McInerney GM, Byth-Wilson K, et al. (2010) A differential role for macropinocytosis in mediating entry of the two forms of vaccinia virus into dendritic cells. PLoS Pathog 6: e1000866.
15. Villa NY, Bartee E, Mohamed MR, Rahman MM, Barrett JW, et al. (2010) Myxoma and vaccinia viruses exploit different mechanisms to enter and infect human cancer cells. Virology 401: 266-279.
16. Huang CY, Lu TY, Bair CH, Chang YS, Jwo JK, et al. (2008) A novel cellular protein, VPEF, facilitates vaccinia virus penetration into HeLa cells through fluid phase endocytosis. J Virol 82: 7988-7999.
17. Law M, Carter GC, Roberts KL, Hollinshead M, Smith GL, (2006) Ligand-induced and non-fusogenic dissolution of a viral membrane. Proc Natl Acad Sci USA 103: 5989-5994.
18. Ichihashi Y, (1996) Extracellular enveloped vaccinia virus escapes neutralization. Virology 217: 478-485.
19. Chung C-S, Hsiao J-C, Chang Y-S, Chang W, (1998) A27L protein mediates vaccinia virus interaction with cell surface heparin sulfate. J Virol 72: 1577-1585.
20. Hsiao JC, Chung CS, Chang W, (1998) Cell surface proteoglycans are necessary for A27L protein- mediated cell fusion: Identification of the N-terminal region of A27L protein as the glycosaminoglycan-binding domain. J Virol 72: 8374-8379.
21. Lin CL, Chung CS, Heine HG, Chang W, (2000) Vaccinia virus envelope H3L protein binds to cell surface heparan sulfate and is important for intracellular mature virion morphogenesis and virus infection in vitro and in vivo. J Virol 74: 3353-3365.
22. Chiu WL, Lin CL, Yang MH, Tzou DLM, Chang W, (2007) Vaccinia virus 4c (A26L) protein on intracellular mature virus binds to the extracellular cellular matrix laminin. J Virol 81: 2149-2157.
23. Ojeda S, Senkevich TG, Moss B, (2006) Entry of vaccinia virus and cell-cell fusion require a highly conserved cysteine-rich membrane protein encoded by the A16L gene. J Virol 80: 51-61.
24. Townsley A, Senkevich TG, Moss B, (2005) Vaccinia virus A21 virion membrane protein is required for cell entry and fusion. J Virol 79: 9458-9469.
25. Senkevich TG, Ward BM, Moss B, (2004) Vaccinia virus A28L gene encodes an essential protein component of the virion membrane with intramolecular disulfide bonds formed by the viral cytoplasmic redox pathway. J Virol 78: 2348-2356.
26. Brown E, Senkevich TG, Moss B, (2006) Vaccinia virus F9 virion membrane protein is required for entry but not virus assembly, in contrast to the related l1 protein. J Virol 80: 9455-9464.
27. Izmailyan RA, Huang CY, Mohammad S, Isaacs SN, Chang W, (2006) The envelope G3L protein is essential for entry of vaccinia virus into host cells. J Virol 80: 8402-8410.
28. Ojeda S, Domi A, Moss B, (2006) Vaccinia virus G9 protein is an essential component of the poxvirus entry-fusion complex. J Virol 80: 9822-9830.
29. Senkevich TG, Moss B, (2005) Vaccinia virus H2 protein is an essential component of a complex involved in virus entry and cell-cell fusion. J Virol 79: 4744-4754.
30. Nichols RJ, Stanitsa E, Unger B, Traktman P, (2008) The vaccinia I2L gene encodes a membrane protein with an essential role in virion entry. J Virol 82: 10247-10261.
31. Senkevich TG, Ojeda S, Townsley A, Nelson GE, Moss B, (2005) Poxvirus multiprotein entry-fusion complex. Proc Natl Acad Sci USA 102: 18572-18577.
32. Bisht H, Weisberg AS, Moss B, (2008) Vaccinia virus L1 protein is required for cell entry and membrane fusion. J Virol 82: 8687-8694.
33. Satheshkumar PS, Moss B, (2009) Characterization of a newly Identified 35 amino acid component of the vaccinia virus entry/fusion complex conserved in all chordopoxviruses. J Virol 83: 12822-12832.
34. Townsley A, Senkevich TG, Moss B, (2005) The product of the vaccinia virus L5R gene is a fourth membrane protein encoded by all poxviruses that is requried for cell entry and cell-cell fusion. J Virol 79: 10988-10998.
35. Condit RC, Moussatche N, Traktman P, (2006) In a nutshell: structure and assembly of the vaccinia virion. Adv Virus Res 66: 31-124.
36. Nelson GE, Wagenaar TR, Moss B, (2008) A conserved sequence within the H2 subunit of the vaccinia virus entry/fusion complex is Important for interaction with the A28 subunit and infectivity. J Virol 82: 6244-6250.
37. Wolfe CL, Moss B, (2011) Interaction between the G3 and L5 proteins of the vaccinia virus entry-fusion complex. Virology 412: 278-283.
38. Wagenaar TR, Ojeda S, Moss B, (2008) Vaccinia virus A56/K2 fusion regulatory protein interacts with the A16 and G9 subunits of the entry fusion complex. J Virol 82: 5153-5160.
39. Loyter A, Citovsky V, Blumenthal R, (1988) The use of fluorescence dequenching measurements to follow viral membrane fusion events. Methods Biochem Anal 33: 129-164.
40. Doms RW, Blumenthal R, Moss B, (1990) Fusion of intra- and extracellular forms of vaccinia virus with the cell membrane. J Virol 64: 4884-4892.
41. Chung CS, Huang CY, Chang W, (2005) Vaccinia virus penetration requires cholesterol and results in specific viral envelope proteins associated with lipid rafts. J Virol 79: 1623-1634.
42. Locker JK, Kuehn A, Schleich S, Rutter G, Hohenberg H, et al. (2000) Entry of the two infectious forms of vaccinia virus at the plasma membrane is signaling-dependent for the IMV but not the EEV. Mol Biol Cell 11: 2497-2511.
43. Limouze J, Straight AF, Mitchison T, Sellers JR, (2004) Specificity of blebbistatin, an inhibitor of myosin II. J Muscle Res Cell Motil 25: 337-341.
44. Lehmann MJ, Sherer NM, Marks CB, Pypaert M, Mothes W, (2005) Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J Cell Biol 170: 317-325.
45. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, et al. (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10: 839-850.
46. Gu C, Yaddanapudi S, Weins A, Osborn T, Reiser J, et al. (2010) Direct dynamin-actin interactions regulate the actin cytoskeleton. EMBO J 29: 3593-3606.
47. Kruchten AE, McNiven MA, (2006) Dynamin as a mover and pincher during cell migration and invasion. J Cell Sci 119: 1683-1690.
48. Praefcke GJ, McMahon HT, (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5: 133-147.
49. Brown SS, Spudich JA, (1981) Mechanism of action of cytochalasin: evidence that it binds to actin filament ends. J Cell Biol 88: 487-491.
50. Yarmola EG, Somasundaram T, Boring TA, Spector I, Bubb MR, (2000) Actin-latrunculin A structure and function. Differential modulation of actin-binding protein function by latrunculin A. J Biol Chem 275: 28120-28127.
51. Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S, et al. (1987) Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 262: 5592-5595.
52. Fry DW, Kraker AJ, McMichael A, Ambroso LA, Nelson JM, et al. (1994) A specific inhibitor of the epidermal growth factor receptor tyrosine kinase. Science 265: 1093-1095.
53. Rijken PJ, Hage WJ, van Bergen en Henegouwen PM, Verkleij AJ, Boonstra J, (1991) Epidermal growth factor induces rapid reorganization of the actin microfilament system in human A431 cells. J Cell Sci 100 (Pt 3): 491-499.
54. Sood CL, Ward JM, Moss B, (2008) Vaccinia virus encodes a small hydrophobic virion membrane protein (I5) that enhances replication and virulence in mice. J Virol 82: 10071-10078.
55. Dales S, Kajioka R, (1964) The cycle of multiplication of vaccinia virus in Earle's strain L cells. I. Uptake and penetration. Virology 24: 278-294.
56. Wolffe EJ, Vijaya S, Moss B, (1995) A myristylated membrane protein encoded by the vaccinia virus L1R open reading frame is the target of potent neutralizing monoclonal antibodies. Virology 211: 53-63.
57. Nelson GE, Sisler JR, Chandran D, Moss B, (2008) Vaccinia virus entry/fusion complex subunit A28 is a target of neutralizing and protective antibodies. Virology 380: 394-401.
58. Kemble GW, Danieli T, White JM, (1994) Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 76: 383-391.
59. Armstrong RT, Kushnir AS, White JM, (2000) The transmembrane domain of influenza hemagglutinin exhibits a stringent length requirement to support the hemifusion to fusion transition. J Cell Biol 151: 425-437.
60. Zavorotinskaya T, Qian Z, Franks J, Albritton LM, (2004) A point mutation in the binding subunit of a retroviral envelope protein arrests virus entry at hemifusion. J Virol 78: 473-481.
61. Zaitseva E, Mittal A, Griffin DE, Chernomordik LV, (2005) Class II fusion protein of alphaviruses drives membrane fusion through the same pathway as class I proteins. J Cell Biol 169: 167-177.
62. Zheng QA, Chang DC, (1991) Reorganization of cytoplasmic structures during cell fusion. J Cell Sci 100 (Pt 3): 431-442.
63. Eitzen G, (2003) Actin remodeling to facilitate membrane fusion. Biochim Biophys Acta 1641: 175-181.
64. Massarwa R, Carmon S, Shilo BZ, Schejter ED, (2007) WIP/WASp-based actin-polymerization machinery is essential for myoblast fusion in Drosophila. Dev Cell 12: 557-569.
65. Kallewaard NL, Bowen AL, Crowe JE Jr, (2005) Cooperativity of actin and microtubule elements during replication of respiratory syncytial virus. Virology 331: 73-81.
66. Gower TL, Pastey MK, Peeples ME, Collins PL, McCurdy LH, et al. (2005) RhoA signaling is required for respiratory syncytial virus-induced syncytium formation and filamentous virion morphology. J Virol 79: 5326-5336.
67. Pontow SE, Heyden NV, Wei S, Ratner L, (2004) Actin cytoskeletal reorganizations and coreceptor-mediated activation of rac during human immunodeficiency virus-induced cell fusion. J Virol 78: 7138-7147.
68. Schowalter RM, Wurth MA, Aguilar HC, Lee B, Moncman CL, et al. (2006) Rho GTPase activity modulates paramyxovirus fusion protein-mediated cell-cell fusion. Virology 350: 323-334.
69. Stantchev TS, Markovic I, Telford WG, Clouse KA, Broder CC, (2007) The tyrosine kinase inhibitor genistein blocks HIV-1 infection in primary human macrophages. Virus Res 123: 178-189.
70. Harmon B, Ratner L, (2008) Induction of the Galpha(q) signaling cascade by the human immunodeficiency virus envelope is required for virus entry. J Virol 82: 9191-9205.
71. Harmon B, Campbell N, Ratner L, (2010) Role of Abl kinase and the Wave2 signaling complex in HIV-1 entry at a post-hemifusion step. PLoS Pathog 6: e1000956.
72. Miyauchi K, Kim Y, Latinovic O, Morozov V, Melikyan GB, (2009) HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 137: 433-444.
73. Phalen T, Kielian M, (1991) Cholesterol is required for infection by Semliki Forest virus. J Cell Biol 112: 615-623.
74. Biswas S, Yin SR, Blank PS, Zimmerberg J, (2008) Cholesterol promotes hemifusion and pore widening in membrane fusion induced by influenza hemagglutinin. J Gen Physiol 131: 503-513.
75. Lustig S, Fogg C, Whitbeck JC, Eisenberg RJ, Cohen GH, et al. (2005) Combinations of polyclonal or monoclonal antibodies to proteins of the outer membranes of the two infectious forms of vaccinia virus protect mice against a lethal respiratory challenge. J Virol 79: 13454-13462.
76. Su HP, Garman SC, Allison TJ, Fogg C, Moss B, et al. (2005) The 1.51-A structure of the poxvirus L1 protein, a target of potent neutralizing antibodies. Proc Natl Acad Sci USA 102: 4240-4245.
77. Su HP, Golden JW, Gittis AG, Hooper JW, Garboczi DN, (2007) Structural basis for the binding of the neutralizing antibody, 7D11, to the poxvirus L1 protein. Virology 368: 331-341.
78. Earl PL, Moss B, (1998) Characterization of recombinant vaccinia viruses and their products. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, editors. Current Protocols in Molecular Biology New York Greene Publishing Associates & Wiley Interscience pp. 16.18.11-16.18.11.
79. Earl PL, Cooper N, Wyatt LS, Moss B, Carroll MW, (1998) Preparation of cell cultures and vaccinia virus stocks. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, editors. Current Protocols in Molecular Biology New York John Wiley and Sons pp. 16.16.11-16.16.13.
80. Earl PL, Moss B, Wyatt LS, Carroll MW, (1998) Generation of recombinant vaccinia viruses. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, editors. Current Protocols in Molecular Biology New York Greene Publishing Associates & Wiley Interscience pp. 16.17.11-16.17.19.